Adaptations, Exaptations, and Spandrels

David M. BussDepartment of
Psychology University of Texas at Austin Martie G.
HaseltonDepartment of Psychology University of Texas at Austin
Todd K. ShackelfordDivision of Science—Psychology Florida
Atlantic University April L. BleskeDepartment of
Psychology University of Texas at Austin Jerome C.
WakefieldSchool of Social Work Rutgers, The State University of New
Jersey

ABSTRACT

Adaptation and natural selection are central concepts in the
emerging science of evolutionary psychology. Natural selection is the only
known causal process capable of producing complex functional organic
mechanisms. These adaptations, along with their incidental by-products and a
residue of noise, comprise all forms of life. Recently, S. J. Gould
(1991) proposed that exaptations and spandrels may be more important than
adaptations for evolutionary psychology. These refer to features that did not
originally arise for their current use but rather were co-opted for new
purposes. He suggested that many important phenomena–such as art, language,
commerce, and war–although evolutionary in origin, are incidental spandrels of
the large human brain. The authors outline the conceptual and evidentiary
standards that apply to adaptations, exaptations, and spandrels and discuss
the relative utility of these concepts for psychological science.

The confusion can be traced to several factors. First, psychologists
typically receive no formal training in evolutionary biology and, therefore,
cannot be expected to wade through what has become a highly technical field.
Second, although evolutionary theorizing about humans has a long history (e.g.,
Baldwin,
1894 ; Darwin,
1859/1958 ; James,
1890/1962 ; Jennings,
1930 ; Morgan, 1896
; Romanes,
1889 ), the empirical examination within psychology of evolutionary
hypotheses regarding human psychological mechanisms is much more recent, and
confusion often inheres in newly emerging approaches as practitioners struggle,
often with many false starts, to use an incipient set of theoretical tools. 1
Third, psychologists dating back to Darwin's time have had
a history of wariness about evolutionary approaches and, therefore, often have
avoided a serious consideration of their potential utility. Fourth, there are
genuine differences in scientific opinion about which concepts should be used,
what the concepts actually mean, and how they should be applied. This article
seeks to provide psychologists with a guide to the basic concepts involved in
the current dispute over evolutionary explanations and to clarify the role that
each of these concepts plays in an evolutionary approach to human psychology.

Darwin's task was more difficult than it might appear at first. He wanted not
only to explain why life-forms have the characteristics they do and why these
characteristics change over time but also to account for the particular ways in
which they change. He wanted to explain how new species emerge (hence the title
of his book, On The Origin of Species by Means of Natural Selection; Darwin,
1859/1958 ) as well as how others vanish. Darwin wanted to explain why the
component parts of animals–the long necks of giraffes, the wings of birds, the
trunks of elephants, and the proportionately large brains of humans–exist in the
particular forms they do. In addition, he wanted to explain the apparent
purposive quality of these complex organic forms, or why they seem to function
to help organisms to accomplish specific tasks.

Darwin's
(1859/1958) answer to all these puzzles of life was the theory of natural
selection. Darwin's theory of natural selection had three essential ingredients:
variation, inheritance, and selection. Animals within a species vary in all
sorts of ways, such as wing length, trunk strength, bone mass, cell structure,
fighting ability, defensive maneuverability, and social cunning. This variation
is essential for the process of evolution to operate. It provides the raw
materials for evolution.

Only some of these variations, however, are reliably passed down from parents
to offspring through successive generations. Other variations, such as a wing
deformity caused by a chance environmental accident, are not inherited by
offspring. Only those variations that are inherited play a role in the
evolutionary process.

The third critical ingredient of Darwin's
(1859/1958) theory was selection. Organisms with particular heritable
attributes produce more offspring, on average, than those lacking these
attributes because these attributes help to solve specific problems and thereby
contribute to reproduction in a particular environment. For example, in an
environment in which the primary food source is nut-bearing trees or bushes,
some finches with a particular shape of beak might be better able to crack nuts
and get at their meat than finches with alternative beak shapes. More finches
that have the beaks better shaped for nut-cracking survive than those with beaks
poorly shaped for nut-cracking. Hence, those finches with more suitably shaped
beaks are more likely, on average, to live long enough to pass on their genes to
the next generation.

Organisms can survive for many years, however, and still fail to contribute
inherited qualities to future generations. To pass on their qualities, they must
reproduce. Differential reproductive success, by virtue of the possession of
heritable variants, is the causal engine of evolution by natural selection.
Because survival is usually necessary for reproduction, survival took on a
critical role in Darwin's
(1859/1958) theory of natural selection.

Darwin
(1859/1958) envisioned two classes of evolved variants–one playing a role in
survival and one playing a role in reproductive competition. For example, among
humans, sweat glands help to maintain a constant body temperature and thus
presumably help humans to survive. Humans' tastes for sugar and fat presumably
helped to guide their ancestors to eat certain foods and to avoid others and
thus helped them to survive. Other inherited attributes aid more directly in
reproductive competition and are said to be sexually selected ( Darwin,
1871/1981 ). The elaborate songs and brilliant plumage of various bird
species, for example, help to attract mates, and hence to reproduce, but may do
nothing to enhance the individual's survival. In fact, these characteristics may
be detrimental to survival by carrying large metabolic costs or by alerting
predators.

In summary, although differential reproductive success of inherited variants
was the crux of Darwin's
(1859/1958) theory of natural selection, he conceived of two classes of
variants that might evolve–those that help organisms survive (and thus
indirectly help them to reproduce) and those that more directly help organisms
in reproductive competition. The theory of natural selection unified all living
creatures, from single-celled amoebas to multicellular mammals, into one grand
tree of descent. It also provided for the first time a scientific theory to
account for the exquisite design and functional nature of the component parts of
each of these species.

In its modern formulation, the evolutionary process of natural selection has
been refined in the form of inclusive fitness theory ( Hamilton,
1964 ). Hamilton reasoned that classical fitness–a measure of an
individual's direct reproductive success in passing on genes through the
production of offspring–was too narrow to describe the process of evolution by
selection. He proposed that a characteristic will be naturally selected if it
causes an organism's genes to be passed on, regardless of whether the organism
directly produces offspring. If a person helps a brother, a sister, or a niece
to reproduce and nurture offspring, for example, by sharing resources, offering
protection, or helping in times of need, then that person contributes to the
reproductive success of his or her own genes because kin tend to share genes
and, moreover, contributes to the reproductive success of genes specifically for
brotherly, sisterly, or niecely assistance (assuming that such helping is partly
heritable and, therefore, such genes are likely to be shared by kin). The
implication of this analysis is that parental care–investing in one's own
children–is merely a special case of caring for kin who carry copies of one's
genes in their bodies. Thus, the notion of classical fitness was expanded to
inclusive fitness.

Technically, inclusive fitness is not a property of an individual organism
but rather a property of its actions or effects ( Hamilton,
1964 ; see also Dawkins,
1982 ). Inclusive fitness can be calculated from an individual's own
reproductive success (classical fitness) plus the effects the individual's
actions have on the reproductive success of his or her genetic relatives,
weighted by the appropriate degree of genetic relatedness.

It is critical to keep in mind that evolution by natural selection is not
forward looking or intentional. A giraffe does not notice juicy leaves stirring
high in a tree and "evolve" a longer neck. Rather, those giraffes that happen to
have slightly longer necks than other giraffes have a slight advantage in
getting to those leaves. Hence, they survive better and are more likely to live
to pass on genes for slightly longer necks to offspring. Natural selection acts
only on those variants that happen to exist. Evolution is not intentional and
cannot look into the future to foresee distant needs.

There has been much debate about the precise meaning of adaptation, but we
offer a provisional working definition. An adaptation may be defined as
an inherited and reliably developing characteristic that came into existence as
a feature of a species through natural selection because it helped to directly
or indirectly facilitate reproduction during the period of its evolution (after
Tooby
& Cosmides, 1992 ). Solving an adaptive problem–that is, the manner in
which a feature contributes to reproduction–is the function of the adaptation.
There must be genes for an adaptation because such genes are required for the
passage of the adaptation from parents to offspring. Adaptations, therefore, are
by definition inherited, although environmental events may play a critical role
in their ontogenetic development.

Ontogenetic events play a profound role in several ways. First, interactions
with features of the environment during ontogeny (e.g., certain placental
nutrients, aspects of parental care) are critical for the reliable development
and emergence of most adaptations. Second, input during development may be
required to activate existing mechanisms. There is some evidence, for example,
that experience in committed sexual relationships activates sex-linked jealousy
adaptations ( Buss,
Larsen, Westen, & Semmelroth, 1992 ). Third, developmental events may
channel individuals into one of several alternative adaptive paths specified by
evolved decision rules. Lack of an investing father during the first several
years of life, for example, may incline individuals toward a short-term mating
strategy, whereas the presence of an investing father may shift individuals
toward a long-term mating strategy (e.g., Belsky,
Steinberg, & Draper, 1991 ; for alternative theories, see Buss &
Schmitt, 1993 ; Gangestad
& Simpson, 1990 ). Fourth, environmental events may disrupt the
emergence of an adaptation in a particular individual, and thus the genes for
the adaptation do not invariantly result in its intact phenotypic manifestation.
Fifth, the environment during development may affect where in the selected range
someone falls, such as which language a person speaks or how anxious a person
tends to be. Developmental context, in short, plays a critical role in the
emergence and activation of adaptations (see DeKay &
Buss, 1992 , for a more extended discussion of the role of context).

To qualify as an adaptation, however, the characteristic must reliably emerge
in reasonably intact form at the appropriate time during an organism's life.
Furthermore, adaptations tend to be typical of most or all members of a species,
with some important exceptions, such as characteristics that are sex-linked,
that exist only in a subset because of frequency-dependent selection, or that
exist because of temporally or spatially varying selection pressures.

Adaptations need not be present at birth. Many adaptations develop long after
birth. Bipedal locomotion is a reliably developing characteristic of humans, but
most humans do not begin to walk until a year after birth. The breasts of women
and a variety of other secondary sex characteristics reliably develop, but they
do not start to develop until puberty.

The characteristics that make it through the filtering process in each
generation generally do so because they contribute to the successful solution of
adaptive problems–solutions that either are necessary for reproduction or
enhance relative reproductive success. Solutions to adaptive problems can be
direct, such as a fear of dangerous snakes that solves a survival problem or a
desire to mate with particular members of one's species that helps to solve a
reproductive problem. They can be indirect, as in a desire to ascend a social
hierarchy, which many years later might give an individual better access to
mates. Or they can be even more indirect, such as when a person helps a brother
or a sister, which eventually helps that sibling to reproduce or nurture
offspring. Adaptive solutions need not invariably solve adaptive problems in
order to evolve. The human propensity to fear snakes, for example, does not
inevitably prevent snakebites, as evidenced by the hundreds of people who die
every year from snakebites ( Than-Than et
al., 1988 ). Rather, adaptive designs must provide reproductive benefits on
average, relative to their costs and relative to alternative designs available
to selection, during the period of their evolution.

Each adaptation has its own period of evolution. Initially, a mutation occurs
in a single individual. Most mutations disrupt the existing design of the
organism and hence hinder reproduction. If the mutation is helpful to
reproduction, however, it will be passed down to the next generation in greater
numbers. In the next generation, therefore, more individuals will possess the
characteristic. Over many generations, if it continues to be successful, the
characteristic will spread among the population. In sum, natural selection is
the central explanatory concept of evolutionary theory, and adaptation refers to
any functional characteristic whose origin or maintenance must be explained by
the process of natural selection. 2

Most adaptations, of course, are not caused by single genes. The human eye,
for example, takes thousands of genes to construct. An adaptation's environment
of evolutionary adaptedness (EEA) refers to the cumulative selection processes
that constructed it piece by piece until it came to characterize the species.
Thus, there is no single EEA that can be localized at a particular point in time
and space. The EEA will differ for each adaptation and is best described as a
statistical aggregate of selection pressures over a particular period of time
that are responsible for the emergence of an adaptation ( Tooby &
Cosmides, 1992 ).

The hallmarks of adaptation are features that define special design
–complexity, economy, efficiency, reliability, precision, and functionality
( Williams,
1966 ). These qualities are conceptual criteria subject to empirical testing
and potential falsification for any particular hypothesis about an adaptation.
Because, in principle, many alternative hypotheses can account for any
particular constellation of findings, a specific hypothesis that a feature is an
adaptation is, in effect, a probability statement that it is highly unlikely
that the complex, reliable, and functional aspects of special design
characterizing the feature could have arisen as an incidental by-product of
another characteristic or by chance alone ( Tooby &
Cosmides, 1992 ). As more and more functional features suggesting special
design are documented for a hypothesized adaptation, each pointing to a
successful solution to a specific adaptive problem, the alternative hypotheses
of chance and incidental by-product become increasingly improbable.

Although adaptations are the primary products of the evolutionary process,
they are not the only products. The evolutionary process also produces
by-products of adaptations as well as a residue of noise. By-products are
characteristics that do not solve adaptive problems and do not have to have
functional design. They are carried along with characteristics that do have
functional design because they happen to be coupled with those adaptations. The
whiteness of bones, for example, is an incidental by-product of the fact that
they contain large amounts of calcium, which was presumably selected because of
properties such as strength rather than because of whiteness (see Symons, 1992
).

An example from the domain of humanly designed artifacts illustrates the
concept of a by-product. Consider a particular lightbulb designed for a reading
lamp; this lightbulb is designed to produce light. Light production is its
function. The design features of a lightbulb–the conducting filament, the vacuum
surrounding the filament, and the glass encasement–all contribute to the
production of light and are part of its functional design. Lightbulbs also
produce heat, however. Heat is a by-product of light production. It is carried
along not because the bulb was designed to produce heat but rather because heat
tends to be a common incidental consequence of light production.

A naturally occurring example of a by-product of adaptation is the human
belly button. There is no evidence that the belly button, per se, helped human
ancestors to survive or reproduce. A belly button is not good for catching food,
detecting predators, avoiding snakes, locating good habitats, or choosing mates.
It does not seem to be involved directly or indirectly in the solution to an
adaptive problem. Rather, the belly button is a by-product of something that is
an adaptation, namely, the umbilical cord that formerly provided the food supply
to the growing fetus. As this example illustrates, establishing the hypothesis
that something is a by-product of an adaptation generally requires the
identification of the adaptation of which it is a by-product and the reason it
is coupled with that adaptation ( Tooby &
Cosmides, 1992 ). In other words, the hypothesis that something is a
by-product, just like the hypothesis that something is an adaptation, must be
subjected to rigorous standards of scientific confirmation and potential
falsification. As we discuss below, incidental by-products may come to have
their own functions or may continue to have no evolved function at all, and they
may be ignored or valued and exploited by people in various cultures.

The third and final product of the evolutionary process is noise, or random
effects. Noise can be produced by mutations that neither contribute to nor
detract from the functional design of the organism. The glass encasement of a
lightbulb, for example, often contains perturbations from smoothness due to
imperfections in the materials and the process of manufacturing that do not
affect the functioning of the bulb; a bulb can function equally well with or
without such perturbations. In self-reproducing systems, these neutral effects
can be carried along and passed down to succeeding generations, as long as they
do not impair the functioning of the mechanisms that are adaptations. Noise is
distinguished from incidental by-products in that it is not linked to the
adaptive aspects of design features but rather is independent of such features.

In summary, the evolutionary process produces three products: naturally
selected features (adaptations), by-products of naturally selected features, and
a residue of noise. In principle, the component parts of a species can be
analyzed, and empirical studies can be conducted to determine which of these
parts are adaptations, which are by-products, and which represent noise.
Evolutionary scientists differ in their estimates of the relative sizes of these
three categories of products. Some argue that many obviously important human
qualities, such as language, are merely incidental by-products of large brains
(e.g., Gould, 1991
). Others argue that qualities such as language show evidence of special
design that render it highly improbable that it is anything other than a
well-designed adaptation for communication and conspecific manipulation ( Pinker, 1994
). Despite these differences among competing scientific views about the
importance and prevalence of adaptations and by-products, all evolutionary
scientists agree that there are many constraints on optimal design.

Adaptationists are sometimes accused of being panglossian, a term
named after Voltaire's
(1759/1939) Pangloss, who proposed that everything was for the best ( Gould &
Lewontin, 1979 ). According to this criticism, adaptationists are presumed
to believe that selection creates optimal design, and practitioners are presumed
to liberally spin adaptationist stories. Humans have noses designed to hold up
eyeglasses and laps designed to hold computers, and they grow bald so that they
can be more easily spotted when lost! This sort of fanciful storytelling,
lacking rigorous standards for hypothesis formulation and evidentiary
evaluation, would be poor science indeed. Although some no doubt succumb to this
sort of cocktail banter, evolutionists going back to Darwin have long recognized
important forces that prevent selection from creating optimally designed
adaptations (see Dawkins,
1982 , for an extensive summary of these constraints).

First, evolution by selection is a slow process, so there will often be a lag
in time between a new adaptive problem and the evolution of a mechanism designed
to solve it. The hedgehog's antipredator strategy of rolling into a ball is
inadequate to deal with the novel impediment to survival created by automobiles.
The moth's mechanism for flying toward light is inadequate for dealing with the
novel challenge to survival of candle flames. The existence in humans of a
preparedness mechanism for developing a fear of snakes may be a relic not well
designed to deal with urban living, which currently contains hostile forces far
more dangerous to human survival (e.g., cars, electrical outlets) but for which
humans lack evolved mechanisms of fear preparedness ( Mineka, 1992
). Because of these evolutionary time lags, humans can be said to live in a
modern world, but they are burdened with a Stone Age brain designed to deal with
ancient adaptive problems, some of which are long forgotten ( Allman, 1994
).

A second constraint on adaptation occurs because of local optima. A better
design may be available, in principle, atop a "neighboring mountain," but
selection cannot reach it if it has to go through a deep fitness valley to get
there. Selection requires that each step and each intermediate form in the
construction of an adaptation be superior to its predecessor form in the
currency of fitness. An evolutionary step toward a better solution would be
stopped in its tracks if that step caused too steep a decrement in fitness.
Selection is not like an engineer who can start from scratch and build toward a
goal. Selection works only with the available materials and has no foresight.
Local optima can prevent the evolution of better adaptive solutions that might,
in principle, exist in potential design space ( Dennett,
1995 ; Williams,
1992 ).

Lack of available genetic variation imposes a third constraint on optimal
design. In the context of artificial selection, for example, it would be
tremendously advantageous for dairy breeders to bias the sex ratio of offspring
toward milk-producing females rather than nonlactating males. But all
selective-breeding attempts to do this have failed, presumably because cattle
lack the requisite genetic variation to bias the sex ratio ( Dawkins,
1982 ). Similarly, it might, in principle, be advantageous for humans to
evolve X-ray vision to see what is on the other side of obstacles or telescopic
vision to spot danger from miles away. But the lack of available genetic
variation, along with other constraints, has apparently precluded such
adaptations.

A fourth constraint centers on the costs involved in the construction of
adaptations. At puberty, male adolescents experience a sharply elevated
production of circulating plasma testosterone. Elevated testosterone is linked
to onset of puberty, an increase in body size, the production of masculine
facial features, and the commencement of sexual interest and activity. But
elevated testosterone also has an unfortunate cost–it compromises the immune
system, rendering men more susceptible than women to a variety of diseases ( Folstad
& Karter, 1992 ; Wedekind,
1992 ). Presumably, averaged over all men through many generations, the
benefits of elevated testosterone outweighed its costs in the currency of
fitness. It evolved despite these costs. The key point is that all adaptations
carry costs–sometimes minimal metabolic costs and at other times large survival
costs–and these costs impose constraints on the optimal design of adaptations.

A fifth class of constraints involves the necessity of coordination with
other mechanisms. Adaptations do not exist in a vacuum, isolated from other
evolved mechanisms. Selection favors mechanisms that coordinate well with, and
facilitate the functioning of, other evolved mechanisms. This process of
coordination, however, often entails compromises in the evolution of an
adaptation that render it less efficient than might be optimal in the absence of
these constraints. Women, for example, have been selected both for bipedal
locomotion and for the capacity for childbirth. The widened hips and birth canal
that facilitate childbirth, however, compromise the ability to locomote with
great speed. Without the need to coordinate design for running with design for
childbirth, selection may have favored slimmer hips like those found on men,
which facilitate running speed. The departure from optimal design for running
speed in women, therefore, presumably occurs because of compromises required by
the need to coordinate adaptive mechanisms with each other. 3
Thus, constraints imposed by the coordination of evolved
mechanisms with each other produce design that is less than might be optimal if
the mechanisms were not required to coexist.

Time lags, local optima, lack of available genetic variation, costs, and
limits imposed by adaptive coordination with other mechanisms all constitute
some of the major constraints on the design of adaptations, but there are others
( Dawkins,
1982 ; Williams,
1992 ). Adaptations are not optimally designed mechanisms. They are better
described as jerry-rigged, meliorative solutions to adaptive problems
constructed out of the available materials at hand, constrained in their quality
and design by a variety of historical and current forces.

Recently, Stephen J.
Gould (1991, 1997b ;
see also Gould &
Lewontin, 1979 ; Gould &
Vrba, 1982 ) proposed that the concept of exaptation is a crucial tool for
evolutionary psychology, providing a critical supplement to the concept of
adaptation. According to this argument, some evolutionary biologists and
psychologists have conflated the historical origins of a mechanism or structure
with its current utility. For example, the feathers of birds may have originated
as evolved mechanisms for thermal regulation. Over evolutionary time, however,
the feathers appear to have been co-opted for a different function–flight.
According to this distinction, the term adaptation would be properly
applied to the original thermal regulation structure and function, but the term
exaptation would be more appropriate for describing the current
flight-producing structure and function.

Gould
(1991) provided two related definitions of exaptations. First, an exaptation
is "a feature, now useful to an organism, that did not arise as an adaptation
for its present role, but was subsequently co-opted for its current function"
(p. 43). Second, exaptations are "features that now enhance fitness, but were
not built by natural selection for their current role" (p. 47). On the basis of
these related definitions, a mechanism must have a function and must enhance the
fitness of its bearer to qualify as an exaptation.

It should be noted that Gould was inconsistent in his usage of the concept of
exaptation, even within a single article (e.g., Gould, 1991
). Although the definitions of exaptation quoted verbatim here appear to
reflect his most common usage (indeed, the quoted 1991 definition was first
introduced by Gould and
Vrba in 1982 ), at other times, he seemed to use the term to cover novel but
functionless uses or consequences of existing characteristics. For conceptual
clarity, it is critical to distinguish between exaptation, as Gould (1991)
defined it in the quoted passages, and by-products that are unrelated to
function in the biological sense. In the next section, we examine Gould's
various usages of the term exaptation. However, in this article, we use
exaptation, consistent with the above quoted definitions, to refer only
to mechanisms that have new biological functions that are not the ones that
caused the original selection of the mechanisms. Biologically functionless uses
are referred to as "effects," "consequences," or "by-products." These two easily
confused strands of Gould's discussion of exaptation are thus disentangled here
and treated separately.

According to Gould (1991)
, exaptations come in two types. In the first type, features that evolved by
selection for one function are co-opted for another function. We use the term
co-opted adaptation to describe this first category. The feathers of
birds first having evolved for thermal regulation but then later co-opted for
flight is an example of a co-opted adaptation. In the second type, "presently
useful characteristics did not arise as adaptations . . . but owe their origin
to side consequences of other features" ( Gould, 1991
, p. 53). Gould called such side effects of the organism's architecture
"spandrels." The term spandrels is an architectural term that refers to
the spaces left over between structural features of a building. The spaces
between the pillars of a bridge, for example, can subsequently be used by
homeless persons for sleeping, even though such spaces were not designed for
providing such shelter.

In sum, Gould (1991)
proposed two types of func- tional exaptations–adaptations that initially
arose through natural selection and were subsequently co-opted for another
function (co-opted adaptations) and features that did not arise as adaptations
through natural selection but rather as side effects of adaptive processes and
that have been co-opted for a biological function (co-opted spandrels). In both
cases, according to Gould's primary definition, a mechanism must possess a
biological function that contributes to fitness to qualify as an exaptation.

As an example of an exaptation, Gould (1991)
used the large size of the human brain and its function of enabling humans
to produce speech. The large brain size, according to his argument, originally
arose as an adaptation for some (unspecified) functions in humans' ancestral
past ( Gould, 1991
). But the complexity of the human brain produces many by-products that are
not properly considered to be functions of the brain: "The human brain, as
nature's most complex and flexible organ, throws up spandrels by the thousands
for each conceivable adaptation in its initial evolutionary restructuring" ( Gould, 1991
, p. 58). Among the spandrels he cited as being by-products of large brains
are religion, reading, writing, fine arts, the norms of commerce, and the
practices of war. These seem to be intended as functionless uses or by-products
rather than true fitness-enhancing, co-opted spandrels. Gould (1991)
concluded that among features of interest to psychologists, such by-products
are "a mountain to the adaptive molehill" (p. 59).

From these arguments, Gould (1991)
concluded that the concepts of exaptations and spandrels provide a "one-line
refutation of . . . an ultra-Darwinian theory based on adaptation" (p. 58). The
two standard pillars of evolutionary biology–natural selection and
adaptation–cannot, in principle, account for human behavior "without fatal
revisions in its basic intent" (p. 58). Note that Gould was not challenging the
importance of evolutionary biology for understanding human behavior. Indeed, as
we show later in this article, understanding the nature of the adaptation
responsible for producing spandrels (in this case, the nature of the large human
brain) is critical to the analysis. Rather, he argued that there has been an
overreliance on explanation in terms of adaptation, and to this important
explanatory concept must be added the concept of exaptation, which is "a crucial
tool for evolutionary psychology" ( Gould, 1991
, p. 43).

Taken literally, Gould's
(1991) cited definition of exaptation requires that a feature be co-opted
for its current function and that it now enhances fitness. It may seem from
these phrases that exaptations concern only functions operating at the present
moment, whether or not they operated in the past. However, evolutionary
psychologists and biologists are generally interested in explaining existing
features of organisms. Obviously, a characteristic cannot be explained by
current fitness-enhancing properties that came about after the characteristic
already existed. When evolutionists attempt to explain the existence of a
feature, they must do so by reference to its evolutionary history. All
evolutionary explanations of the existence of species-wide mechanisms are to
this extent explanations in terms of the past fitness effects of that kind of
mechanism that led to the current existence of the mechanism in the species. The
fact that a mechanism currently enhances fitness, by itself, cannot explain why
the mechanism exists or how it is structured ( Tooby &
Cosmides, 1990b ).

There are good reasons to think that it is not scientifically illuminating to
demonstrate a feature's current correlation with fitness ( Symons, 1992
; Tooby &
Cosmides, 1990b ), unless such correlations reveal longer term, past
selective pressures. It is not clear that such correlations shed any light on
the mechanism's design or status as an adaptation. Such correlations may reveal
the current direction of selection, although even this assumes that such
correlations will continue to be obtained in future generations–a questionable
assumption given the rapidly changing biotic and abiotic environments.
Evolutionary explanation focuses on explaining why a feature exists, not what
incidental interactions the feature may be having with the current environment.

Confusion 3: Current Functions Versus Past Functions That Are No Longer
Active

Another confusion lurking in Gould's
(1991) language is that it seems to imply that the past functions that
explain the existence of a mechanism must still be operating now and literally
be a current function to be an adaptation or exaptation. The concepts of
adaptation and exaptation are intended as explanatory concepts, and they may be
explanatorily useful even when the cited functions are no longer operative.
Selected features often cease having the fitness-enhancing effects that got them
selected in the first place; for example, it is possible that a selected taste
for fatty foods to ensure adequate caloric intake is no longer fitness-enhancing
in industrial societies where excessive fat is harmfully common and available
for consumption. When evolutionists attempt to explain why humans have a taste
for fatty foods, however, they generally say that this taste likely is (or was)
an adaptation to ensure adequate caloric intake. Current fitness enhancement is
not at issue; at issue is the past function explaining the existence of the
mechanisms behind the taste for fatty foods.

A similar point holds for an exaptation. For example, if birds that fly
subsequently were to become nonflying, so their feathers would no longer have
the exapted function of supporting flight, the existence of feathers at that
future time would still need to be explained in terms of (a) an original
adaptation for heat insulation and (b) a later exaptation for flying, followed
by (c) a functionless period too short for feathers to be selected out. So, the
use of exaptation as an evolutionary explanatory concept does not require that
there be a current function, any more than the use of adaptation requires such a
current function. However, the use of exaptation requires, as Gould (1991)
was trying to convey, that there be an original function and a distinct
later function (he appeared to use "current" to conveniently distinguish the
later function from the original function). What is required for exaptational
explanation is not that there be an active current function but that there was
an active function at the time that the feature is claimed to have served as an
exaptation.

Confusion 4: Function Versus Functionless By-product

The most central confusion in applying Gould's
(1991) ideas pertains to distinguishing between exaptations, as Gould
defined them, and the novel use of existing features that are currently
unrelated to function and fitness. Although Gould (1991)
defined an exaptation as a feature "coopted for its current function" (p.
43) and features that "now enhance fitness, but were not built by natural
selection for their current role" (p. 46), he sometimes argued that "function"
does not describe the utility of exaptations; instead, he suggested that the
utility of an exaptation is better described as "effect" (p. 48). Even more
confusing, he referred to "culturally useful features" (p. 58) of the brain as
exaptations. Gould's stated definitions seem to require that these effects and
culturally useful features must contribute to fitness and have specifiable
biological functions to qualify as exaptations, but it seems implausible that
Gould intended to claim that such cultural practices as reading and writing are
explainable by biological functions. Accordingly, exaptations must be
distinguished from novel uses of existing mechanisms, where the novel uses are
not explained by a biological function.

Consider the human hand as an adaptation. Clearly, the human hand is now used
for many activities that were not part of its original set of functions–playing
handball or disc golf, manipulating a joystick on a Super Nintendo game, or
writing a computer program by pecking on a keyboard. But it seems unlikely that
Gould
(1991) meant to claim that these activities serve any functions in the
formal sense, as solutions to adaptive problems that contribute to reproduction,
although they certainly serve functions in the colloquial meaning of the
term–helping to achieve some goal (e.g., staying in shape, engaging in a
stimulating and distracting activity). The same problem arises for many of the
activities enumerated by Gould as hypothesized exaptations of the large human
brain. Indeed, many of the features Gould claimed to be exaptations or spandrels
in human behavior do not seem to fall under his own definitions of exaptation or
spandrel and seem instead to be functionless by-products. The key point is that
novel uses of existing mechanisms that are not explained by biological function
or fitness (i.e., functionless by-products) must be distinguished from true
functional exaptations, such as the feathers of birds co-opted for flight.

Confusion 5: What Causal Process or Mechanism Is Doing the Co-opting?

Intimately related to the confusion between exaptations and functionless
by-products is a confusion pertaining to the causal process responsible for
co-opting an existing structure (see Pinker,
1997a ). In the example of birds' feathers, which were originally evolved
for thermal regulation but subsequently co-opted for flight, it is clearly
natural selection that is responsible for transforming an existing structure
into a new, modified structure with a different function. In other cases,
however, Gould (1991)
appeared to imply that human psychological capacities, such as cognitive
capacities, human instrumental actions, or motivational mechanisms, are
responsible for the co-opting.

The distinction that evolutionary psychologists make between underlying
mechanisms and manifest behavior is helpful in clarifying this confusion. Both
adaptations and exaptations, as underlying mechanisms, may be subsequently used
for novel behaviors that may have no functional relevance whatsoever. When
people use their hands to grip a tennis racquet, for example, this
evolutionarily recent manifest behavior is clearly not the function for which
the hands evolved. A full understanding of this novel behavior, however,
requires an understanding of the underlying mechanism that is used (the hand)
and is aided by insight into the functions for which it was designed (e.g., the
power grip). The activity (e.g., tennis) may be partially understood by invoking
evolved motivational mechanisms (e.g, social networking, hierarchy negotiation,
enhancement of appearance) that are responsible for humans co-opting or
exploiting existing mechanisms to pursue this novel activity.

In this example, human motivational mechanisms conjoined with current
cognitive and physical capacities, not natural selection, are responsible for
co-opting the existing mechanism of the hand. The same logic applies to many of
Gould's
(1991) other examples of exaptations, such as reading and writing–these are
evolutionarily novel activities that are presumably too recent to have been
co-opted by natural selection and so apparently must have been invented and
co-opted by existing human psychological mechanisms. Such human co-optation must
be distinguished from biological exaptations that natural selection has
transformed from one function to another.

In summary, evolutionary functional analysis is useful regardless of whether
natural selection or some other causal process, such as an existing human
motivation, is responsible for the co-opting. Even in cases where a feature has
no biological function and is proposed to be a functionless by-product, an
understanding of novel behaviors must involve (a) an understanding of the
evolved mechanisms that make humans capable of performing the behavior and (b)
an understanding of the evolved cognitive and motivational mechanisms that led
humans to exploit such capabilities. It is not sufficient from a scientific
point of view to merely present a long speculative list of purported
exaptations, however interesting or intuitively compelling they might be.

The hypothesis that something is an exaptation or even a functionless effect
should be subjected to reasonable standards of hypothesis formulation and
empirical verification, just as hypotheses about adaptation must meet these
standards. The hypothesis that religion, to use one of Gould's
(1991) examples, is an exaptation would seem to require a specification of
(a) the original adaptations or by-products that were co-opted to produce
religion; (b) the causal mechanism responsible for the co-opting (e.g., natural
selection or an existing motivational mechanism); and (c) the exapted biological
function of religion, if any; that is, the manner in which it contributes to the
solution to an adaptive problem of survival or reproduction. These predictions
can then be subjected to evidentiary standards of empirical testing and
potential falsification.

Hypotheses about functionless by-products must meet rigorous scientific
standards that include a functional analysis of the original adaptations
responsible for producing the functionless by-products and the existing human
cognitive and motivational mechanisms responsible for the co-opting. Without
this specification, the mere assertion that this or that characteristic is an
exaptation encounters the same problem that Gould (1991)
leveled against adaptationists–the telling of "just-so stories."

Confusion 6: Are Exaptations Merely Adaptations?

A final conceptual issue pertains to whether the concept of exaptation is
usefully distinct from the concept of adaptation. Dennett
(1995) argued that it is not: According to orthodox Darwinism, every
adaptation is one sort of exaptation or the other–this is trivial, since no
function is eternal; if you go back far enough, you will find that every
adaptation has developed out of predecessor structures each of which either had
some other use or no use at all. (p. 281)\ If all adaptations are exaptations,
and all exaptations are adaptations, then having two terms to describe one thing
would certainly be superfluous.

Although Dennett's
(1995) argument has some merit in pointing to the limits of the distinction
between adaptation and exaptation, we think he is wrong in suggesting that there
is no difference, and we believe that there is utility in differentiating
between the two concepts. Granted, the distinction may end up being more a
matter of degree than an absolute distinction because exaptations themselves
often involve further adaptations; nonetheless, understanding the degree to
which a new function is superimposed on a predecessor structure that already
existed as an adaptation or as a by-product may indeed shed light on its nature.
The notion that a bird's feathers originally were designed for thermal
regulation rather than for flying, for example, may help to explain some of its
current features that do not seem to contribute to flight (e.g., insulating,
heat-retention features).

In sum, Gould's
(1991) concept of exaptation can be meaningfully distinguished from
adaptation. Both concepts invoke function; therefore, both must meet the
conceptual and evidentiary standards for invoking function. The concepts differ,
however, in that adaptations are characteristics that spread through the
population because they were selected for some functional effect, whereas
exaptations are structures that already exist in the population and continue to
exist, albeit sometimes in modified form, for functional reasons different from
the ones for which they were originally selected.

Some readers of Gould
(1997a) come away believing that the role of natural selection is somehow
diminished to the degree that exaptations are important. This is a mistake, as
Gould himself took pains to point out: "I accept natural selection as the only
known cause of 'eminently workable design' and . . . 'adaptive design must be
the product of natural selection' " (p. 57). Natural selection plays a key role
in both adaptations and exaptations.

When exaptations are co-opted adaptations, where the mechanism being co-opted
for a new function was an adaptation, selection is required to explain the
original adaptation being co-opted. Fishes' fins designed for swimming may have
been co-opted to produce mammalian legs for walking. Birds' feathers, perhaps
originally designed for thermal regulation, may have been co-opted for flying.
In all these cases, however, natural selection is required to explain the
origins and nature of the adaptations that provided the existing structures
capable of being co-opted.

When exaptations are co-opted spandrels, where the mechanism being co-opted
for a new function was not an adaptation but rather an incidental by-product of
an adaptation, then selection is required to explain the adaptation that
produced the incidental by-product. Recall that the hypothesis that a mechanism
with a function is a spandrel implies that the mechanism was a by-product, and
supporting a by-product hypothesis generally requires specifying the adaptation
responsible for producing the by-product ( Tooby &
Cosmides, 1992 ). Natural selection is required to explain the origin and
design of the adaptation–it is the only known causal process capable of
producing adaptation. Without specifying the origin of the adaptation that
produced the by-product that was co-opted to become a spandrel, the hypothesis
that something is a spandrel generally cannot be tested.

Selection is necessary not only to explain the adaptations and by-products
that are available for co-optation but also to explain the process of exaptation
itself. Selection is required to explain the structural changes in an existing
mechanism that enable it to perform the new exapted function: "Exaptations
almost always involve structural changes that enable the preexisting mechanism,
designed for another function, to perform the new function; these changes
require explanation by natural selection" ( Wakefield,
in press ). When feathers for thermal regulation become wings capable of
flight, it is highly unlikely that the new function can occur without any
modification of the original mechanism. Selection would have to act on the
existing feathers, favoring those individuals that possess more aerodynamic
features over those possessing less aerodynamic features. Furthermore, these
changes would have to be coordinated with other changes, such as a musculature
capable of generating sufficient flapping, alterations in the visual system to
accommodate the new demands of aerial mobility, and perhaps modifications of the
feet to facilitate landing without damage (e.g., a redesigned shape of the
feet). All these changes require the invocation of natural selection to explain
the transformation of the original adaptation to an exaptation (e.g., an
adaptation with a new function). Similar explanations would generally be
necessary for explaining how functionless by-products are transformed into
co-opted spandrels that perform specific functions.

Selection is also required to explain the maintenance of an exaptation over
evolutionary time, even if no changes in structure occur: "Even in rare cases
where exaptations involve no structural changes whatsoever, selective pressures
must be invoked to fully explain why the mechanism is maintained in the
population" ( Wakefield,
in press ). The forces of selection, of course, are never static. The fact
that more than 99% of all species that have ever existed are now extinct is
harsh testimony to the changes in selection over time ( Thiessen,
1996 ). If the selection pressure responsible for the original adaptation
becomes neutral or reversed, then the adaptation will eventually degrade over
time because of forces such as the cumulative influx of new mutations and
competing metabolic demands of other mechanisms. Selection is not only the force
responsible for the origins of complex mechanisms but also the force responsible
for their maintenance. Thus, even in the odd event that an existing mechanism is
co-opted for a new function with no change whatsoever, selection is required to
explain why this mechanism and its new function are maintained in the population
over time.

In summary, adding exaptation to the conceptual toolbox of evolutionary
psychology does not diminish the importance of natural selection as the primary
process responsible for creating complex organic design–a point apparently
endorsed by all sides involved in these conceptual debates. Selection is
responsible for producing the original adaptations that are then available for
co-optation. It is responsible for producing the adaptations, of which spandrels
are incidental by-products. It is responsible for producing structural changes
in exaptations in order to fulfill their new functions. And it is responsible
for maintaining exaptations in the population over evolutionary time, even in
the rare cases where no structural changes occurred. The distinctions between
exaptation and adaptation are important, and Gould (1991)
deserves credit for highlighting them. However, the distinctions should not
be taken to mean that natural selection is not the basic explanatory principle
in biology and evolutionary psychology.

When a particular hypothesis about an evolved mechanism fails to be supported
empirically, then a number of options are available to researchers. First, the
hypothesis may be right but may have been tested incorrectly. Second, the
hypothesis may be wrong, but an alternative functional hypothesis could be
formulated and tested. Third, the phenomenon under examination might not
represent an adaptation or exaptation at all but might instead be an incidental
by-product of some other evolved mechanism, and this hypothesis could be tested.

Researchers then can empirically test these alternatives. Suppose, for
example, that the sperm transport hypothesis of the female orgasm turned out to
be wrong, with the results showing that women who had orgasms were no more
likely to conceive than were women who did not have orgasms. The researchers
could first scrutinize the methodology to see whether some flaw in the research
design may have gone undetected (e.g., had the researchers controlled for the
ages of the women in the two groups, because inadvertent age differences may
have concealed the effect?). Second, the researchers could formulate an
alternative hypothesis–perhaps the female orgasm functions as a mate selection
device, providing a cue to the woman about the quality of the man or his
investment in her (see Rancour-Laferriere,
1985 , for a discussion of this and other hypotheses about the female
orgasm)–and this alternative could be tested. Third, the researchers could
hypothesize that the female orgasm is not an adaptation at all but rather an
incidental by-product of some other mechanism, such as a common design shared
with men, who do possess the capacity for orgasm for functional reasons (see Symons, 1979
, for the original proposal of this functionless by-product hypothesis, and
Gould's,
1987 , subsequent endorsement of this hypothesis). In this case, researchers
could try to disconfirm all existing functional explanations and could try to
identify how the known mechanisms for development of naturally selected male
orgasmic capacities led to the female orgasmic capacities as a side effect.
Different researchers undoubtedly will have different proclivities about which
of these options they pursue. The key point is that all evolutionary
hypotheses–whether about adaptations, exaptations, spandrels, or functionless
by-products–should be formulated in a precise enough manner to produce empirical
predictions that can then be subjected to testing and potential falsification.

It should be noted that evolutionary hypotheses range on a gradient from
well-formulated, precise deductions from known evolutionary principles on the
one hand to evolutionarily inspired hunches on the other (see, e.g., Symons, 1992
). Evolutionary psychology often provides a heuristic, guiding scientific
inquiry to important domains that have a priori importance, such as events
surrounding reproduction (e.g., sexuality, mate selection). Just as with a
precise evolutionary hypothesis, an evolutionary hunch may turn out to be right
or wrong. It would seem reasonable to hypothesize, for example, that men would
have evolved mechanisms designed to detect when women ovulate, because such a
mechanism would help to solve the adaptive problems of identifying fecund women
and channeling mating effort more efficiently. But there is little solid
empirical evidence that such a mechanism exists (see Symons, 1995
). Such hunches, however, can often be useful in guiding investigations.
Thus, evolutionary psychology, at its best, has both heuristic and predictive
value for psychological science.

In principle, we agree with Gould's
(1991, 1997b)
suggestion to be pluralistic about the conceptual tools of evolutionary
psychology, although it is clear that many evolutionary psychologists already
embody the pluralism advocated (e.g., Tooby &
Cosmides, 1990a , 1992 ).
Researchers may differ about which of these tools they believe are most
scientifically valuable for particular purposes. One reasonable standard for
judging the value of such conceptual tools is the heuristic and predictive
empirical harvest they yield. Table 1
shows 30 recent examples of the empirical findings about humans whose
discovery was guided by hypotheses anchored in adaptation and natural selection.

From this empirical evidence, hypotheses about adaptations appear to have
considerable value. In some cases, adaptation-minded researchers have generated
and tested specific empirical predictions not generated from nonadaptationist
theories, such as sex-linked causes of divorce ( Betzig, 1989
), causes of the intensity of mate retention effort ( Buss &
Shackelford, 1997 ), predictable conditions under which spousal homicide
occurs ( Daly &
Wilson, 1988 ), sex differences in the nature of sexual fantasy ( Ellis &
Symons, 1990 ), and shifts in mate preferences across the life span ( Kenrick
& Keefe, 1992 ). In other cases, adaptation-mindedness has proved
heuristic, guiding researchers to important domains not previously examined or
discovered, such as the role of symmetry in mate attraction ( Thornhill
& Gangestad, 1993 ), the role of deception in mate attraction ( Tooke &
Camire, 1991 ), and the specific conflicts of interest that occur in
stepfamilies ( Wilson &
Daly, 1987 ). Using the same criterion, we could not find a single example
of an empirical discovery made about humans as a result of using the concepts of
exaptations or spandrels (but see MacNeilage,
1997 , for a testable exaptation hypothesis about the origins of human
speech production). Of course, this relative lack of fruitfulness at this time
does not imply that over time, the concepts of exaptation and spandrels cannot
be useful in generating scientific hypotheses and producing empirical
discoveries.

In this article, we have attempted to elucidate the defining criteria of
adaptations, exaptations, spandrels, and functionless by-products. Tables 2 and
3 summarize several important conceptual and evidentiary standards applicable to
each of these concepts.

Adaptations and exaptations–in the form of either co-opted adaptations or
co-opted spandrels–share several common features. All invoke selection at some
point in the causal sequence. All invoke function. All must meet conceptual
criteria for the proposed function–the hallmarks of special design, including
specialization of function for solving a particular adaptive problem. And all
must meet evidentiary standards, such as generating specific testable empirical
predictions and parsimoniously accounting for known empirical findings.

These concepts differ, however, in the role of selective origins and fitness
in explaining a feature. Although all three invoke selection, adaptations that
arose de novo from mutations invoke selection in the original construction of
the mechanism as a species-wide feature. Co-opted adaptations invoke selection
in the original construction of the mechanism that is co-opted as well as in any
reconstruction necessary for reshaping the mechanism for its new function and in
maintaining the mechanism in the population because of its new function. And
co-opted spandrels invoke selection in explaining the adaptations of which they
are by-products, in explaining the reshaping of the by-product for its new
function, and in explaining the maintenance of the by-product in the population
because of its new function. Consequently, relative to initial adaptations,
exaptations carry the additional evidentiary burden of showing that a current
function is distinct from an earlier function or from a functional original
structure.

The most important differences, however, center on the temporal aspect of
function and fitness. Adaptations exist in the present because their form was
shaped in the past by selection for a particular function ( Darwin,
1859/1958 ; Symons, 1979
; Tooby &
Cosmides, 1990b ; Williams,
1966 ). Exaptations, in contrast, exist in the present because they were
co-opted from previous structures that evolved for reasons different from those
of the later exapted function ( Gould, 1991
). Although all three concepts require documentation of special design for a
hypothesized function, co-opted exaptations and spandrels carry the additional
evidentiary burdens of documenting both later co-opted functionality and a
distinct original adaptational functionality. To our knowledge, none of the
items on Gould's
(1991) list of proposed spandrels and exaptations–language, religion,
principles of commerce, warfare, reading, writing, and fine arts–have met these
standards of evidence. Moreover, even if they did meet such standards, this
would in no way diminish the need to place such items within an overall
evolutionary framework in order to adequately understand and explain them–a
point agreed on by all sides of these debates.

Evolutionary psychology is emerging as a promising theoretical perspective
within psychology. As with many emerging theoretical perspectives, there is
often controversy about the meaning and scientific utility of the new
explanatory concepts. Although most psychologists cannot be expected to become
steeped in all of the formal complexities of the highly technical discipline of
evolutionary theory, we hope that this article will serve as a guide to some of
the most theoretically useful core concepts and some of the most interesting
controversies within this emerging perspective in psychological science.